Long-Term Oncologic Outcomes from Laparoscopic Gastrectomy for Gastric Cancer: A Single-Center

Long-Term Oncologic Outcomes from Laparoscopic
Gastrectomy for Gastric Cancer: A Single-Center
Experience of 601 Consecutive Resections
Sang-Woong Lee, MD, Eiji Nomura, MD, George Bouras, MRCS, Takaya Tokuhara, MD,
Souichiro Tsunemi, MD, Nobuhiko Tanigawa, MD, FACS
Laparoscopic gastrectomy (LG) is becoming increasingly popular for management of early
gastric cancer (EGC). Although short-term efficacy is proven, reports on long-term effectiveness are still infrequent.
STUDY DESIGN: All patients with a diagnosis of gastric cancer undergoing LG from the beginning of our
laparoscopic experience were included in the analysis. At our unit, LG is indicated for all cancers
up to preoperative stage T2N1.
RESULTS:
Six-hundred and one laparoscopic resections were included in the analysis. There were 392 men and
209 women. Mean age was 64.2 ⫾ 10.9 years. Distal gastrectomy was performed in 305 patients,
pylorus-preserving gastrectomy in 148, segmental gastrectomy in 42, proximal gastrectomy in 53,
total gastrectomy in 27, and wedge resection in 26. Histological staging revealed that 478 patients
had stage IA disease, 47 had stage IB, 44 had stage IIA, 19 had stage IIB, 8 had stage IIIA, 3 had stage
IIIB, and 2 had stage IIIC. Morbidity and mortality rates were 17.6% and 0.3%, respectively.
Median follow-up was 35.9 months (range 3 to 113 months). Cancer recurrence occurred in 15
patients and metachronous gastric remnant cancer was detected in 6 patients. The 5-year overall and
disease-free survival rates were 94.2% and 89.9%, respectively, for stage IA tumors, 87.4% and
82.7% for stage IB, 80.8% and 70.7% for stage IIA, and 69.6% and 63.1% for stage IIB.
CONCLUSIONS: In our experience, long-term oncological outcomes from LG for EGC are acceptable. Wherever
expertise permits, LG should be considered as the primary treatment in patients with EGC.
(J Am Coll Surg 2010;211:33–40. © 2010 by the American College of Surgeons)
BACKGROUND:
Since its introduction by Kitano and colleagues in 1994,1
the number of patients undergoing laparoscopic gastrectomy (LG) for early gastric cancer (EGC) has been increasing rapidly in Japan, where there is a high incidence of
EGC. Improvements in instruments and laparoscopic
technique have allowed for widespread acceptance of LG,
not only for distal gastrectomy (DG) but also for other
resections, such as proximal gastrectomy (PG) and total
gastrectomy (TG).2-5 Advantages of LG over conventional
open resection include reduced postoperative pain, earlier
recovery, shorter hospital stay, and better cosmesis.6-10 Although there is high-quality evidence to support short-term
efficacy of LG for EGC, accounts on long-term survival are
still infrequent. The technical feasibility of systematic laparoscopic lymphadenectomy must still be proven in the longterm, and concerns about this approach, such as the oncological effects of pneumoperitoneum, must still be resolved.11,12
Detailed and organized accounts of the long-term oncological
efficacy of the LG are necessary to establish this approach as
the primary treatment for EGC. Here we present the longterm oncological outcomes from LG, including all patients
treated from the beginning of our laparoscopic experience, to
determine its long-term effectiveness and patient survival in
the context of EGC.
Disclosure information: Nothing to disclose.
Received February 1, 2010; Revised March 12, 2010; Accepted March 12,
2010.
From the Department of General and Gastroenterological Surgery, Osaka
Medical College, Takatsuki, Japan (Lee, Nomura, Tokuhara, Tsunemi, Tanigawa) and Upper Gastrointestinal Surgery Unit, Queen Elizabeth Hospital,
Edgbaston, Birmingham, UK (Bouras).
Correspondence address: Nobuhiko Tanigawa, MD, FACS, Department of
General and Gastroenterological Surgery, Osaka Medical College, 2-7
Daigaku-Machi, Takatsuki, Osaka 569-8686, Japan. email: sur001@poh.
osaka-med.ac.jp
© 2010 by the American College of Surgeons
Published by Elsevier Inc.
METHODS
Patients
From April 2000 to October 2009, 1,386 patients with
gastric cancer were managed surgically at our unit. Of
these, 601 patients underwent LG.
33
ISSN 1072-7515/10/$36.00
doi:10.1016/j.jamcollsurg.2010.03.018
34
Lee et al
Oncologic Results of Laparoscopic Gastrectomy
J Am Coll Surg
Abbreviations and Acronyms
DG ⫽
EGC ⫽
LG ⫽
PG ⫽
PPG ⫽
SG ⫽
TG ⫽
distal gastrectomy
early gastric cancer
laparoscopic gastrectomy
proximal gastrectomy
pylorus-preserving gastrectomy
segmental gastrectomy
total gastrectomy
Preoperative staging was based on double-contrast upper
gastrointestinal x-ray studies, endoscopy, and enhanced
CT. Indications for LG at our institute include all tumors
confined to the muscularis propria not amenable to endoscopic mucosal resection with lymph node involvement
limited to N1. Patients requiring salvage surgery after incomplete endoscopic resection are also included. Operations were converted to open when serosal invasion or extensive lymphadenopathy was detected at laparoscopy.
Operative procedure
The type of gastric resection was determined according to
tumor location, size, and depth of invasion. Modified (limited) gastrectomy with preservation of remnant stomach is
indicated for EGC based on Japanese treatment guidelines.13 Pylorus-preserving gastrectomy (PPG) and segmental gastrectomy (SG) are indicated for lesions of the
body of stomach limited to the mucosa ⬍4 cm in diameter
and submucosa ⬍2 cm. For PPG, enough distal remnant
to allow for an antral cuff of at least 4 cm for gastrogastric
anastomosis is necessary, and for SG, the right gastroepiploic vessels are preserved to supply a large remnant distal
stomach.14,15 PG is indicated for lesions in the upper third
of stomach with no evidence of serosal or lymph node
involvement.4,16 TG is indicated for locally advanced proximal lesions or multiple lesions for which the distal stomach cannot be preserved.3,17 Finally, wedge resection is indicated for mucosal cancers of any histological type
measuring ⬍2 cm in diameter with a low probability of
regional lymph node metastases.18,19
The principle of any resection is to achieve en-bloc resection of gastric segment and surrounding lymph nodes to
achieve adequate oncological clearance. DG is the most
commonly performed resection at our unit. The patient is
positioned with hips extended and abducted for the primary surgeon, who stands between the legs. Pneumoperitoneum at 8 mmHg is established through a supraumbilical trocar and liver retraction is achieved using a Penrose
drain (Fig. 1). Greater curvature mobilization is performed
by dividing the gastrocolic ligament just away from gastroepiploic arcade. The left gastroepiploic vessels are divided
Figure 1. Penrose drain liver retractor in position in the abdominal
cavity.
to reach the proximal resection line, and the distal mobilization is performed up to the duodenum and the right
gastroepiploic vessels. After duodenal transection, the right
and left gastric vessels are divided and the lesser curve is
cleared of its perigastric fat before gastric transection.
Lymph node dissection is performed during vascular mobilization according to guidelines taking lymph nodes en
bloc on the side of the resection. Vessels are ligated at their
roots in most instances. D1⫹␣ (station nos. 7 and 8a)
lymph node dissection is performed for cancer limited to
the mucosa, and D1⫹␤ (station nos. 7, 8a, and 9) is performed for those thought to be extending submucosally
(Fig. 2). The proximal stomach is divided after confirming
the position of the marking tattoo. The specimen is retrieved from the umbilical trocar site in a bag. Reconstruction is by either Billroth-I (Fig. 3A) or Roux-en-Y (Fig. 3B),
as determined by size of remnant stomach and potential for
tension with a gastroduodenostomy. Intracorporeal anastomoses are fashioned using endoscopic linear staplers.20,21
Follow-up
Histological staging was according to the 7th edition of the
Union Internationale Contre le Cancer stage classification
criteria. Adjuvant chemotherapy in the form of S-1, an oral
fluoropyrimidine, was administered for 1 year in patients
with disease stage higher than IIA.22 All patients were
followed-up prospectively every 6 months for clinical examination and tumor marker measurements (CEA, carbohydrate antigen 19-9), and CT and endoscopy were performed annually.
Statistical analysis
All statistical tests were performed using the JMP 8 for
Windows (SAS Institute Inc.). Differences in categorical
Vol. 211, No. 1, July 2010
Lee et al
Oncologic Results of Laparoscopic Gastrectomy
35
Figure 2. Dissected lymph nodes for D1⫹ ␤ during distal
gastrectomy.
variables, such as postoperative complications, tumor recurrence, and other clinicopathological factors were analyzed by chi-square test and p value ⬍0.05 was considered
significant. Patient survival was calculated by KaplanMeier method. All continuous data are presented as mean
with standard deviations.
RESULTS
Patient characteristics
Demographic, operative, and clinicopathological characteristics of patients undergoing LG are presented in Tables
1 and 2.
Types of laparoscopic resections
Laparoscopic resections consisted of 305 (50.7%) DG, 148
(24.6%) PPG, 42 (7.0%) SG, 53 (8.8%) PG, 27 (4.5%)
TG, and 26 (4.3%) wedge resection. Resections were performed either as laparoscopy-assisted, where the gastric
transection and reconstruction were performed through
minilaparotomy, or totally laparoscopic, where mobilization, resection, and reconstruction were performed intracorporeally. Most of the procedures in our early experience
were laparoscopy-assisted but, since November 2003, we
have been introducing total laparoscopic procedures
starting with stapled intracorporeal reconstruction after
DG.20,21
Concomitant resections of other organs were performed
in 56 cases (9.3%). This included 35 cholecystectomies for
gallstones, 11 colonic resections, 3 rectal resections, 3 oopherectomies for cystic tumors of the ovary, 2 splenecto-
Figure 3. (A) Diagram showing intracorporeal stapled Billroth-I reconstruction. (B) Diagram showing intracorporeal stapled Roux-en-Y
reconstruction.
36
Lee et al
Oncologic Results of Laparoscopic Gastrectomy
Table 1. Demographic, Operative and Tumor Characteristics
of 601 Patients after Laparoscopic Radical Gastrectomy
Patients
Age, y*
Gender, male/female, n
Body mass index*
Operation
Totally laparoscopic procedure,
yes/no, n
Type of gastrectomy, DG/PPG/
SG/PG/TG/WR, n
Lymph node dissection, D0/D1/
D1⫹␣/D1⫹␤/D2, n
Lymph node yields,* n
Resection of other organs, yes/no, n
Operation time, min*
Tumor
Location, U/M/L/W, n
Histology, differentiated/
undifferentiated, n
Tumor size, cm*
Staging,† IA/IB/IIA/IIB/IIIA/IIIB/
IIIC, n
64.2 ⫾ 10.9
392/209
22.4 ⫾ 3.1
297/304
305/148/42/53/27/26
26/42/144/316/73
23.8 ⫾ 13.2
56/545
300.6 ⫾ 84.8
86/320/191/4
342/259
3.2 ⫾ 2.4
478/47/44/19/8/3/2
*Continuous variables are presented as the mean ⫾ standard deviation.
†
Tumor staging is classified by Union Internationale Contre le Cancer
staging.
DG, distal gastrectomy; L, low; M, middle; PG, proximal gastrectomy; PPG,
pylorus-preserving gastrectomy; SG, segmental gastrectomy; TG, total gastrectomy; U, upper; W, whole; WR, wedge resection.
mies as part of D2 dissection, and 2 herniorrhaphies. Some
patients were understaged preoperatively, 45 patients had
T3-stage disease and 8 patients had T4a-stage disease on
histology. Consequently, the final Union Internationale
Contre le Cancer stages of the patients were stage IA in 478
(79.5%), stage IB in 47 (7.8%), stage IIA in 44 (7.3%),
stage IIB in 19 (3.2%), stage IIIA in 8 (1.3%), stage IIIB in
3 (0.5%) and stage IIIC in 2 (0.3%) patients.
Morbidity and mortality
Conversion to open surgery occurred in 31 cases (5.2%)
because of advanced-stage disease in 9 patients, uncontrollable hemorrhage in 7 patients, peritoneal adhesions in 4
J Am Coll Surg
patients, suspected positive proximal resection margins in 3
patients, and jejunal loop torsion during Roux-en-Y reconstruction after DG in 1 patient.
Table 3 summarizes the intraoperative and postoperative
complications according to type of resection. Intraoperative and postoperative complications occurred in 106 patients (17.6%). There were no associations between the
occurrence of complications and demographic factors including gender, age, body mass index, or tumor stage.
There were no statistical differences in the incidence of
intraoperative complications between different types of resections. Bleeding was the most frequent intraoperative
complication. Postoperative complications occurred more
frequently after TG and PG (p ⬍ 0.05). Notably, patients
undergoing TG had a high rate of pancreatic injury
(11.1%) and anastomotic leakage (11.1%). Overall, anastomotic or duodenal stump leakage occurred in 23 patients
(3.8%). Leakage after esophagojejunostomy using a circular stapler and handsewn gastroduodenostomy through
minilaparotomy occurred in 7 and 4 patients, respectively.
Six of these patients required reoperation, and 17 patients
had collections that were treated by percutaneous drainage.
Gastric stasis occurred in 10 (6.8%) of 148 patients treated
with PPG. On contrary, gastric stasis after SG was seen in
only 1 (2.4%) of 42 patients. Four patients suffered from
postoperative hemorrhage associated with pancreatic inflammation and secondary pseudoaneurysm of the gastroduodenal artery in 3 patients and splenic artery in 1. All
patients were successfully treated by endovascular coiling.
Two patients died postoperatively (0.3%), 1 from severe
acute pancreatitis and another from acute respiratory distress syndrome.
Follow-up
Median follow-up was 35.9 months (range 3 to 113
months). Distant recurrences occurred in 14 (2.3%) patients, including 8 peritoneal, 4 hepatic, 1 para-aortic, and
1 bone recurrence (Table 4). A left upper quadrant port site
recurrence developed 2 years after surgery in 1 patient with
stage IIIC (T3N3) disease and was treated with chemotherapy. A bone metastasis developed 4 years after resection in
Table 2. Stage Grouping of 601 Patients after Laparoscopic Radical Gastrectomy
T1 (mucosa, submucosa), n
T2 (muscularis propria), n
T3 (subserosa), n
T4a (serosa), n
T4b (adjacent structure), n
n (%)
N0 (0)
N1 (1ⴚ2)
N2 (3ⴚ6)
N3 (7ⴚ)
n
%
478
24
25
3
0
530 (88.2)
23
9
13
3
0
48 (8.0)
10
3
4
0
0
17 (2.8)
0
1
3
2
0
6 (1.0)
511
37
45
8
0
601
85.0
6.2
7.5
1.3
2
100
Staging according to the 7th edition of the Union Internationale Contre le Cancer classification.
Vol. 211, No. 1, July 2010
Lee et al
Oncologic Results of Laparoscopic Gastrectomy
37
Table 3. Intraoperative and Postoperative Complications in 601 Patients Undergoing Laparoscopic Radical Gastrectomy
Complications
Morbidity*
Intraoperative, n (%)
Bleeding, n
Organ injury, n
Postoperative, n (%)
Anastomotic leakage, n
Duodenal stump leakage, n
Anastomotic stricture, n
Anastomotic ulcer, n
Stasis, n
Pancreatic injury, n
Bleeding, n
Bowel obstruction, n
Wound infection, n
Pulmonary infection, n
Mortality
ARDS, n
Severe pancreatitis, n
Type of resection
SG (n ⴝ 42) PG (n ⴝ 53)
DG (n ⴝ 305)
PPG (n ⴝ 148)
5 (1.6)
4
1
60 (19.7)
9
3
3
3
8
16
3
2
10
3
0
0
0
25 (16.9)
2
0
2
2
10
4
1
0
3
1
1 (2.4)
1
0
7 (16.7)
2
0
0
0
1
2
0
0
2
0
0
1
0
0
0
0
TG (n ⴝ 27)
WR (n ⴝ 26)
p Value
1 (1.9)
1
0
17 (32.1)
4
0
2
0
3
2
1
1
2
2
1 (3.7)
1
0
10 (37.0)
3
0
1
0
0
3
0
0
2
1
0
0
0
3 (11.5)
0
0
0
1
0
0
0
0
1
1
NS
0
0
1
0
0
0
⬍0.05†
*There were 130 complications in 106 patients.
†
Statistical significance.
DG, distal gastrectomy; PG, proximal gastrectomy; PPG, pylorus-preserving gastrectomy; SG, segmental gastrectomy; TG, total gastrectomy; WR, wedge
resection.
1 patient with stage IA disease, but with a mucosal lesion
measuring 90 mm with no lymph node metastases. Four
patients underwent palliative reoperation and chemotherapy and an additional 8 received chemotherapy only. The
resection margin was positive in 1 case after wedge resection. Local recurrence in the gastric remnant eventually
developed in this patient and was treated with DG. Metachronous gastric remnant cancer was encountered in 6 pa-
Table 4. Details of Patients with Distant and Local Recurrences after Laparoscopic Radical Gastrectomy
Pathologic findings of primary disease
Patient
no.
Age,
y/gender
Type
of LG
Intervals
after LG,
mos
Recurrence
site
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
56/female
66/female
73/female
67/male
46/female
57/male
69/male
63/male
75/male
57/female
68/male
77/male
69/male
46/female
82/male
DG
PG
PG
DG
TG
PG
PG
DG
WR
DG
DG
SG
DG
DG
WR
30
35
6
46
6
24
7
48
11
27
23
29
5
24
5
P
P
P
Bone
H
N
P
H/N
H
P/N
P
P
H
Port/P
Locoregional
His.
Size,
mm
Depth of invasion
ly
V
N
Stage
Tub
Tub
Por
Tub
Por
Pap
Tub
Tub
Tub
Por
Por
Por
Tub
Por
Tub
150
34
95
90
20
45
30
34
16
60
195
39
20
60
23
Subserosa
Submucosa
Serosa
Mucosa
Submucosa
Muscularis propria
Muscularis propria
Muscularis propria
Muscularis propria
Submucosa
Subserosa
Muscularis propria
Muscularis propria
Serosa
Submucosa
(⫹)
(⫹)
(⫹)
(⫺)
(⫹)
(⫹)
(⫹)
(⫹)
(⫹)
(⫹)
(⫹)
(⫹)
(⫺)
(⫹)
(⫹)
(⫺)
(⫹)
(⫹)
(⫺)
(⫺)
(⫹)
(⫹)
(⫹)
(⫹)
(⫺)
(⫺)
(⫹)
(⫹)
(⫹)
(⫹)
N3
N2
N0
N0
N2
N1
N0
N3
N0
N1
N1
N2
N1
N3
N0
IIIB
IIA
IIB
IA
IIA
IIA
IB
IIIA
IB
IB
IIB
IIB
IIA
IIIC
IA
DG, distal gastrectomy; H, liver; LG, laparoscopic gastrectomy; ly, lymphatic invasion; PG, proximal gastrectomy; P, peritoneal disease; Pap, papillary
adenocarcinoma; Por, poorly differentiated adenocarcinoma; Port, port site; SG, segmental gastrectomy; TG, total gastrectomy; Tub, tubular adenocarcinoma;
V, venous invasion; WR, wedge resection.
38
Lee et al
Oncologic Results of Laparoscopic Gastrectomy
Figure 4. Kaplan-Meier overall survival curves according to tumor
stage based on the 7th edition of the Union Internationale Contre le
Cancer classification. Eleven patients with stage III disease have
been omitted because of small sample size.
tients (1.0%). Three of these underwent partial resection of
the remnant stomach, 2 patients had total gastrectomies
and 1 patient had endoscopic submucosal dissection of the
second lesion. Another primary cancer developed in 17
patients during the follow-up period, and 33 patients died
in total. Causes of death included recurrent disease in 11
patients, another primary cancer in 6, chronic pulmonary
disease in 4, cardiovascular disease in 2, apoplexy in 2,
chronic liver dysfunction in 2, surgery-related complications in 2, diabetes mellitus in 1, chronic renal failure in 1,
collagen disease in 1, and systemic infection in 1. Of 601
patients, 181 were followed-up for ⬎5 years or until death.
In these patients, 5-year overall and disease-free survival
rates were 90.3% and 85.3%, respectively. According to
stage, 5-year overall and disease-free survival rates were
94.2% and 89.9% for 478 stage IA disease, 87.4% and
82.7% for 47 stage IB disease, 80.8% and 70.7% for 44
stage IIA disease, and 69.6% and 63.1% for 19 stage IIB
disease, respectively (Figs. 4 and 5). According to the depth
of tumor invasion, 5-year overall survival rates were 93.4%
for 511 T1 tumors, 70.0% for 37 T2 tumors, 76.7% for 45
T3 tumors, and 57.1% for 8 T4a tumor (Fig. 6).
Figure 6. Kaplan-Meier overall survival curves according to T stage
based on the 7th edition of the Union Internationale Contre le Cancer
classification.
J Am Coll Surg
Figure 5. Kaplan-Meier disease-free survival curves according to
tumor stage based on the 7th edition of the Union Internationale
Contre le Cancer classification. Eleven patients with stage III disease have been omitted because of small sample size.
DISCUSSION
Several prospective trials have demonstrated LG to be superior to open surgery because it results in less postoperative pain, faster recovery, and better cosmetic results.7-10 In
light of proven short-term efficacy, the current series represents the largest of its kind investigating the long-term
effectiveness of LG in the treatment of gastric cancer stages
I and II. In the present cohort, operative morbidity and
mortality rates were 17.6% and 0.3%, respectively, and
comparable with other accounts in the literature reporting
complication rates ranging from 2.5% to 26.7%.23-31 Conversion to open operation occurred for oncological reasons
as well as after intraoperative complications, but conversion itself was not associated with poor outcomes. Pancreatic inflammation can be secondary to laparoscopic energy
devices transmitting heat and causing pancreatic injury
during radical lymph node dissection. Such injury can lead
to development of serious complications, including anastomotic leakage and hemorrhage that can require surgical
or radiological intervention.
A particular problem encountered in the current series
was the understaging of 8.8% of cases (53 of 601). Although comparable with other reports,2,25,26 such patients
with histologically advanced disease had poor outcomes.
The inadvertent application of LG in such patients is difficult to avoid, however, as there is still an uncertainty
about the oncological efficacy of laparoscopic manipulation in serosa-positive disease, all efforts must be made to
prevent preoperative and intraoperative understaging to
apply conventional open measures of preventing peritoneal
seedling in advanced disease.11,32
The 5-year overall survival rate for the 511 patients with
EGC was 93.4% and comparable with accounts of open
resection.33-35 Other authors have also published data supporting the oncological efficacy of LG when compared
with open resection in EGC.23,28 Although the uncharac-
Vol. 211, No. 1, July 2010
teristic distant recurrence in a patient with T1N0 cancer 4
years after surgery raises some concern, such superficially
spreading tumors have been known to have a high frequency of metastasis.36 In the present cohort, cancer recurrence developed in 4 patients with EGC (0.8%): 1 hepatic,
1 boney, and 2 peritoneal. These oncological outcomes are
comparable with other accounts supporting the oncological efficacy of LG in EGC.33,37,38 For patients in whom
metachronous gastric cancers developed, 5 lesions would
have been present before the original resection but were not
detected because they were presumably too small. In accordance with the literature, additional surgical resection of
the second cancer was beneficial to survival.39-41
Kitano and colleagues, in a multicenter retrospective
study of 1,294 LGs in 16 institutions, reported that the
morbidity and mortality rates were 14.8% and 0%, respectively, and 5-year disease-free survival rate was 99.8% for
stage IA disease, 98.7% for stage IB disease, and 85.7% for
stage II disease with a median follow-up of 36 months.27
The seemingly excellent long-term survival of this cohort is
overshadowed by concerns about missing data and patients
lost to follow-up. Fujiwara and colleagues, in a singlecenter study of 94 LGs for EGC, reported that the morbidity and mortality rates were 22.3% and 0%, respectively, and overall survival rate was 90.1%.25 Similar to our
experience, such figures might be more realistic benchmarks for LG when applied to EGC.
In conclusion, LG for EGC appears safe and feasible
with acceptable short-term surgical and long-term oncological outcomes. Based on this evidence, wherever expertise permits, LG should be considered as the primary treatment in patients with EGC. Curative resection for
advanced disease is technically possible, however, the current data cannot address oncological efficacy in these patients. The role of LG in advanced disease must be evaluated prospectively in a randomized controlled setting.
Author Contributions
Study conception and design: Lee, Nomura, Tanigawa
Acquisition of data: Lee, Nomura, Bouras, Tokuhara, Tsunemi, Tanigawa
Analysis and interpretation of data: Lee, Nomura, Bouras
Drafting of manuscript: Lee, Bouras, Tanigawa
Critical revision: Lee, Nomura, Bouras, Tokuhara, Tanigawa
REFERENCES
1. Kitano S, Iso Y, Moriyama M, Sugimachi K. Laparoscopyassisted Billroth I gastrectomy. Surg Laparosc Endosc 1994;4:
146–148.
Lee et al
Oncologic Results of Laparoscopic Gastrectomy
39
2. Asao T, Hosouchi Y, Nakabayashi T, et al. Laparoscopically assisted total or distal gastrectomy with lymph node dissection for
early gastric cancer. Br J Surg 2001;88:128–132.
3. Mochiki E, Kamimura H, Haga N, et al. The technique of
laparoscopically assisted total gastrectomy with jejunal interposition for early gastric cancer. Surg Endosc 2002;16:540–544.
4. Tanimura S, Higashino M, Fukunaga Y, et al. Laparoscopic
gastrectomy with regional lymph node dissection for upper gastric cancer. Br J Surg 2007;94:204–207.
5. Uyama I, Sugioka A, Matsui H, et al. Laparoscopic side-to-side
esophagogastrostomy using a linear stapler after proximal gastrectomy. Gastric Cancer 2001;4:98–102.
6. Adachi Y, Suematsu T, Shiraishi N, et al. Quality of life after
laparoscopy-assisted Billroth I gastrectomy. Ann Surg 1999;229:
49–54.
7. Mochiki E, Nakabayashi T, Kamimura H, et al. Gastrointestinal
recovery and outcome after laparoscopy-assisted versus conventional open distal gastrectomy for early gastric cancer. World
J Surg 2002;26:1145–1149.
8. Reyes CD, Weber KJ, Gagner M, Divino CM. Laparoscopic vs
open gastrectomy. A retrospective review. Surg Endosc 2001;15:
928–931.
9. Kitano S, Shiraishi N, Fujii K, et al. A randomized controlled
trial comparing open vs laparoscopy-assisted distal gastrectomy
for the treatment of early gastric cancer: an interim report. Surgery 2002;131[Suppl]:S306–S311.
10. Adachi Y, Shiraishi N, Shiromizu A, et al. Laparoscopy-assisted
Billroth I gastrectomy compared with conventional open gastrectomy. Arch Surg 2000;135:806–810.
11. Volz J, Koster S, Spacek Z, Paweletz N. The influence of pneumoperitoneum used in laparoscopic surgery on an intraabdominal tumor growth. Cancer 1999;86:770–774.
12. Maehara Y, Hasuda S, Koga T, et al. Postoperative outcome and
sites of recurrence in patients following curative resection of
gastric cancer. Br J Surg 2000;87:353–357.
13. The Japanese Gastric Cancer Society. Guidelines for Diagnosis
and Treatment of Carcinoma of the Stomach. 2nd English edition (April 2004). Available at: URL: http://www.jgca.jp/
PDFfiles/Guidelines2004_eng.pdf. Accessed May 7, 2010.
14. Shinohara H, Sonoda T, Niki M, et al. Laparoscopically-assisted
pylorus-preserving gastrectomy with preservation of the vagus
nerve. Eur J Surg 2002;168:55–58.
15. Lee SW, Bouras G, Nomura E, et al. Intracorporeal stapled
anastomosis following laparoscopic segmental gastrectomy for
gastric cancer: technical report and surgical outcomes. Surg Endosc 2009. [Epub ahead of print].
16. Uyama I, Sugioka A, Fujita J, et al. Completely laparoscopic
proximal gastrectomy with jejunal interposition and lymphadenectomy. J Am Coll Surg 2000;191:114–119.
17. Mochiki E, Toyomasu Y, Ogata K, et al. Laparoscopically assisted total gastrectomy with lymph node dissection for upper
and middle gastric cancer. Surg Endosc 2008;22:1997–2002.
18. Ohgami M, Otani Y, Kumai K, et al. Curative laparoscopic
surgery for early gastric cancer: five years experience. World
J Surg 1999;23:187–192; discussion 192–183.
19. Nozaki I, Kubo Y, Kurita A, et al. Long-term outcome after
laparoscopic wedge resection for early gastric cancer. Surg Endosc 2008;22:2665–2669.
20. Kanaya S, Gomi T, Momoi H, et al. Delta-shaped anastomosis
in totally laparoscopic Billroth I gastrectomy: new technique of
intraabdominal gastroduodenostomy. J Am Coll Surg 2002;
195:284–287.
40
Lee et al
Oncologic Results of Laparoscopic Gastrectomy
21. Takaori K, Nomura E, Mabuchi H, et al. A secure technique of
intracorporeal Roux-Y reconstruction after laparoscopic distal
gastrectomy. Am J Surg 2005;189:178–183.
22. Sakuramoto S, Sasako M, Yamaguchi T, et al. Adjuvant chemotherapy for gastric cancer with S-1, an oral fluoropyrimidine.
N Engl J Med 2007;357:1810–1820.
23. Mochiki E, Kamiyama Y, Aihara R, et al. Laparoscopic assisted
distal gastrectomy for early gastric cancer: five years’ experience.
Surgery 2005;137:317–322.
24. Kitano S, Shiraishi N, Kakisako K, et al. Laparoscopy-assisted
Billroth-I gastrectomy (LADG) for cancer: our 10 years’ experience. Surg Laparosc Endosc Percutan Tech 2002;12:204–207.
25. Fujiwara M, Kodera Y, Misawa K, et al. A. Longterm outcomes of early-stage gastric carcinoma patients treated with
laparoscopy-assisted surgery. J Am Coll Surg 2008;206:138–
143.
26. Fujiwara M, Kodera Y, Miura S, et al. Laparoscopy-assisted distal gastrectomy with systemic lymph node dissection: a phase II study following the learning curve. J Surg Oncol 2005;91:26–32.
27. Kitano S, Shiraishi N, Uyama I, et al. A multicenter study on
oncologic outcome of laparoscopic gastrectomy for early cancer
in Japan. Ann Surg 2007;245:68–72.
28. Huscher CG, Mingoli A, Sgarzini G, et al. Laparoscopic versus
open subtotal gastrectomy for distal gastric cancer: five-year results of a randomized prospective trial. Ann Surg 2005;241:
232–237.
29. Kim MC, Kim HH, Jung GJ. Surgical outcome of laparoscopyassisted gastrectomy with extraperigastric lymph node dissection
for gastric cancer. Eur J Surg Oncol 2005;31:401–405.
30. Kim MC, Jung GJ, Kim HH. Morbidity and mortality of
laparoscopy-assisted gastrectomy with extraperigastric lymph node
dissection for gastric cancer. Dig Dis Sci 2007;52:543–548.
J Am Coll Surg
31. Shimizu S, Noshiro H, Nagai E, et al. Laparoscopic gastric surgery in a Japanese institution: analysis of the initial 100 procedures. J Am Coll Surg 2003;197:372–378.
32. Lee YJ, Ha WS, et al. Port-site recurrence after laparoscopyassisted gastrectomy: report of the first case. J Laparoendosc Adv
Surg Tech A 2007;17:455–457.
33. Maruyama K, Sasako M, Kinoshita T, et al. Surgical treatment
for gastric cancer: the Japanese approach. Semin Oncol 1996;
23:360–368.
34. Siewert JR, Sendler A. The current management of gastric cancer. Adv Surg 1999;33:69–93.
35. Isozaki H, Tanaka N, Okajima K. General and specific prognostic factors of early gastric carcinoma treated with curative surgery. Hepatogastroenterology 1999;46:1800–1808.
36. Yasuda K, Inomata M, Fujii K, et al. Superficially spreading
cancer of the stomach. Ann Surg Oncol 2002;9:192–196.
37. Sano T, Sasako M, Kinoshita T, Maruyama K. Recurrence of
early gastric cancer. Follow-up of 1475 patients and review of
the Japanese literature. Cancer 1993;72:3174–3178.
38. Saka M, Katai H, Fukagawa T, et al. Recurrence in early gastric
cancer with lymph node metastasis. Gastric Cancer 2008;11:
214–218.
39. Sasako M, Maruyama K, Kinoshita T, Okabayashi K. Surgical
treatment of carcinoma of the gastric stump. Br J Surg 1991;78:
822–824.
40. Isozaki H, Tanaka N, Fujii K, et al. Surgical treatment for advanced carcinoma of the gastric remnant. Hepatogastroenterology 1998;45:1896–1900.
41. Newman E, Brennan MF, Hochwald SN, et al. Gastric remnant
carcinoma: just another proximal gastric cancer or a unique
entity? Am J Surg 1997;173:292–297.